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Changes in volatiles in carrots inoculated with ACC deaminase-producing bacteria isolated from organic crops

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An Erratum to this article was published on 30 March 2016

Abstract

Aims

Bacterial ACC deaminase is one of the key tools to ameliorate plant stress by lowering ethylene level in plants. The effects of ACC deaminase-producing bacteria on the volatile profiles in plants have not been examined to date. To address this, we performed metabolic profiling of volatiles in carrots following inoculation of the bacteria producing ACC deaminase.

Methods

We isolated ACC deaminase-producing bacteria from the inner part of the fruits and vegetables grown on organic farms by culturing on ACC-containing media, and screened them with PCR for the acdS gene, mungbean growth assay, and in vitro ACC deaminase activity. The isolated endophytes were evaluated for their ability to alter volatile profiles in carrots.

Results

Eleven bacterial strains possessing the activity to cleave ACC were selected among the 60 isolates grown on the medium containing ACC as a sole N source. Three of them that belonged to Pseudomonas could reduce the levels of (E)-2-hexenal and the other green leaf volatiles (GLVs) and terpenoids in the carrot leaves following inoculation of the seeds.

Conclusions

The isolated endophytes with ACC deaminase activity could alter the composition of volatiles in plants, probably through lowering ethylene level in the plant.

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References

  • Arimura G, Ozawa R, Nishioka T, Boland W, Koch T, Kühnemann F, Takabayashi J (2002) Herbivore‐induced volatiles induce the emission of ethylene in neighboring lima bean plants. Plant J 29:87–98

    Article  CAS  PubMed  Google Scholar 

  • Arimura G, Garms S, Maffei M, Bossi S, Schulze B, Leitner M, Mithöfer A, Boland W (2008) Herbivore-induced terpenoid emission in Medicago truncatula: concerted action of jasmonate, ethylene and calcium signaling. Planta 227:453–464

    Article  CAS  PubMed  Google Scholar 

  • Arimura G, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiol 50:911–923

    Article  CAS  PubMed  Google Scholar 

  • Arimura G, Ozawa R, Maffei ME (2011) Reacent advances in plant early signaling in response to herbivory. Int J Mol Sci 12:3723–3739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arshad M, Saleem M, Hussain S (2007) Perspectives of bacterial ACC deaminase in phytoremediation. Trends Biotechnol 25:356–362

    Article  CAS  PubMed  Google Scholar 

  • Belimov AA, Safronova VI, Sergeyeva TA, Egorova TN, Matveyeva VA, Tsyganov VE, Borisov AY, Tikhonovich IA, Kluge C, Preisfeld A (2001) Characterization of plant growth promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol 47:642–652

    Article  CAS  PubMed  Google Scholar 

  • Blaha D, Prigent-Combaret C, Mirza MS, Moënne-Loccoz Y (2006) Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol 56:455–470

    Article  CAS  PubMed  Google Scholar 

  • Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838

    Article  CAS  PubMed  Google Scholar 

  • Croft KPC, Juttner F, Slusarenko AJ (1993) Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiol 101:13–24

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dell’Amico E, Cavalca L, Andreoni V (2008) Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 40:74–84

    Article  Google Scholar 

  • Dworkin M, Foster J (1958) Experiments with some microorganisms which utilize ethane and hydrogen. J Bacteriol 75:592

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fukuda T, Okazaki K, Shinano T (2013) Aroma characteristic and volatile profiling of carrot varieties and quantitative role of terpenoid compounds for carrot sensory attributes. J Food Sci 78:1800–1806

    Article  Google Scholar 

  • Ghosh S, Penterman JN, Little RD, Chavez R, Glick BR (2003) Three newly isolated plant growth-promoting bacilli facilitate the seedling growth of canola, Brassica campestris. Plant Physiol Biochem 41:277–281

    Article  CAS  Google Scholar 

  • Glick BR (2004) Bacterial ACC deaminase and the alleviation of plant stress. Adv Appl Microbiol 56:291–312

    Article  CAS  PubMed  Google Scholar 

  • Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7

    Article  CAS  PubMed  Google Scholar 

  • Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39

    Article  CAS  PubMed  Google Scholar 

  • Glick BR, Karaturovíc DM, Newell PC (1995) A novel procedure for rapid isolation of plant growth promoting pseudomonads. Can J Microbiol 41:533–536

    Article  CAS  Google Scholar 

  • Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the Salkowski Reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon SA, Weber RP (1951) Colorimetric estimation of indole acetic acid. Plant Physiol 26:192–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biol Biochem 37:395–412

    Article  CAS  Google Scholar 

  • Gray WM, Ostin A, Sandberg G, Romano CP, Estelle M (1998) High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc Natl Acad Sci U S A 95:7197–7202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gurska J, Wang W, Gerhardt KE, Khalid AM, Isherwood DM, Huang X-D, Glick BR, Greenberg BM (2009) Three year field test of a plant growth promoting rhizobacteria enhanced phytoremediation system at a land farm for treatment of hydrocarbon waste. Environ Sci Technol 43:4472–4479

    Article  CAS  PubMed  Google Scholar 

  • Hallmann J, Quadt-Hallmann A, Mahaffee W, Kloepper J (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914

    Article  CAS  Google Scholar 

  • Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471

    Article  CAS  PubMed  Google Scholar 

  • Honma M, Shimomura T (1978) Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric Biol Chem 42:1825–1831

    CAS  Google Scholar 

  • Hontzeas N, Richardson A, Belimov A, Safronova V, Abu-Omar M, Glick B (2005) Evidence for horizontal transfer of 1-aminocyclopropane-1-carboxylate deaminase genes. Appl Environ Microbiol 71:7556–7558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hynes RK, Leung GC, Hirkala DL, Nelson LM (2008) Isolation, selection, and characterization of beneficial rhizobacteria from pea, lentil, and chickpea grown in western Canada. Can J Microbiol 54:248–258

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa M, Nakajima K, Yanagi M, Yamamoto Y, Yamasato K (2003) Marinilactibacillus psychrotolerans gen. nov., sp nov., a halophilic and alkaliphilic marine lactic acid bacterium isolated from marine organisms in temperate and subtropical areas of Japan. Int J Syst Evol Microbiol 53:711–720

    Article  CAS  PubMed  Google Scholar 

  • Jalili F, Khavazi K, Pazira E, Nejati A, Rahmani HA, Sadaghiani HR, Miransari M (2009) Isolation and characterization of ACC deaminase-producing fluorescent pseudomonads, to alleviate salinity stress on canola (Brassica napus L.) growth. J Plant Physiol 166:667–674

    Article  CAS  PubMed  Google Scholar 

  • Kachroo A, Kachroo P (2009) Fatty acid-derived signals in plant defense. Annu Rev Phytopathol 47:153–176

    Article  CAS  PubMed  Google Scholar 

  • Kjeldsen F, Christensen LP, Edelenbos M (2003) Changes in volatile compounds of carrots (Daucus carota L.) during refrigerated and frozen storage. J Agric Food Chem 51:5400–5407

    Article  CAS  PubMed  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Sa T (2007) Characterization of 1-aminocyclopropane-1-carboxylate (ACC) deaminase containing Methylobacterium oryzae and interactions with auxins and ACC regulation of ethylene in canola (Brassica campestris). Planta 226:867–876

    Article  CAS  PubMed  Google Scholar 

  • Maffei M (2010) Sites of synthesis, biochemistry and functional role of plant volatiles. S Afr J Bot 76:612–631

    Article  CAS  Google Scholar 

  • Maimaiti J, Zhang Y, Yang J, Cen YP, Layzell DB, Peoples M, Dong Z (2007) Isolation and characterization of hydrogen-oxidizing bacteria induced following exposure of soil to hydrogen gas and their impact on plant growth. Environ Microbiol 9:435–444

    Article  CAS  PubMed  Google Scholar 

  • Marques APGC, Pires C, Moreira H, Rangel AOSS, Castro PML (2010) Assessment of the plant growth promotion abilities of six bacterial isolates using Zea mays as indicator plant. Soil Biol Biochem 42:1229–1235

    Article  CAS  Google Scholar 

  • Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol 9:274–280

    Article  CAS  PubMed  Google Scholar 

  • Matsui K, Minami A, Hornung E, Shibata H, Kishimoto K, Ahnert V, Kindl H, Kajiwara T, Feussner I (2006) Biosynthesis of fatty acid derived aldehydes is induced upon mechanical wounding and its products show fungicidal activities in cucumber. Phytochemistry 67:649–657

    Article  CAS  PubMed  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530

    Article  CAS  Google Scholar 

  • Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195

    Article  CAS  PubMed  Google Scholar 

  • Nascimento FX, Rossi MJ, Soares CR, McConkey BJ, Glick BR (2014) New insights into 1-aminocyclopropane-1-carboxylate (ACC) deaminase phylogeny, evolution and ecological significance. PLoS One 9, e99168

    Article  PubMed  PubMed Central  Google Scholar 

  • Ozawa R, Shiojiri K, Kishimoto K, Matsui K, Arimura G-i, Urashimo S, Nishioka T, Takabayashi J (2013) Cytosolic LOX overexpression in Arabidopsis enhances the attractiveness of parasitic wasps in response to herbivory and incidences of parasitism. J Plant Interact 8:207–215

    Article  CAS  Google Scholar 

  • Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase‐containing plant growth‐promoting rhizobacteria. Physiol Plant 118:10–15

    Article  CAS  PubMed  Google Scholar 

  • Penrose DM, Moffatt BA, Glick BR (2001) Determination of 1-aminocycopropane-1-carboxylic acid (ACC) to assess the effects of ACC deaminase-containing bacteria on roots of canola seedlings. Can J Microbiol 47:77–80

    Article  CAS  PubMed  Google Scholar 

  • Rashid S, Charles TC, Glick BR (2012) Isolation and characterization of new plant growth-promoting bacterial endophytes. Appl Soil Ecol 61:217–224

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Saravanakumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102:1283–1292

    Article  CAS  PubMed  Google Scholar 

  • Sekizawa Y, Haruyama T, Kano H, Urushizaki S, Saka H, Matsumoto K, Haga M (1990) Dependence on ethylene of the induction of peroxidase and lipoxygenase activity in rice leaf infected with blast fungus. Agric Biol Chem 54:471–478

    CAS  Google Scholar 

  • Seljåsen R, Hoftun H, Bengtsson GB (2001) Sensory quality of ethylene-exposed carrots (Daucus carota L, cv ‘Yukon’) related to the contents of 6-methoxymellein, terpenes and sugars. J Sci Food Agric 81:54–61

    Article  Google Scholar 

  • Shaharoona B, Arshad M, Khalid A (2007) Differential response of etiolated pea seedlings to inoculation with rhizobacteria capable of utilizing 1-aminocyclopropane-1-carboxylate or L-methionine. J Microbiol 45:15–20

    CAS  PubMed  Google Scholar 

  • Siddikee MA, Chauhan PS, Anandham R, Han G-H, Sa T (2010) Isolation, characterization, and use for plant growth promotion under salt stress, of ACC deaminase-producing halotolerant bacteria derived from coastal soil. J Microbiol Biotechnol 20:1577–1584

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H (2013) Auxin biology in roots. Plant Roots 7:49–64

    Article  CAS  Google Scholar 

  • Talcott S, Howard L (1999) Chemical and sensory quality of processed carrot puree as influenced by stress-induced phenolic compounds. J Agric Food Chem 47:1362–1366

    Article  CAS  PubMed  Google Scholar 

  • Timmusk S, Paalme V, Pavlicek T, Bergquist J, Vangala A, Danilas T, Nevo E (2011) Bacterial distribution in the rhizosphere of wild barley under contrasting microclimates. PLoS One 6, e17968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van de Poel B, Van Der Straeten D (2014) 1-aminocyclopropane-1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene! Front Plant Sci 640:1–11

    Google Scholar 

  • Van de Poel B, Smet D, Van Der Straeten D (2015) Ethylene and hormonal cross talk in vegetative growth and development. Plant Physiol 169:61–72

    Article  PubMed  PubMed Central  Google Scholar 

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586

    Article  CAS  Google Scholar 

  • Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283–291

    Article  CAS  PubMed  Google Scholar 

  • Watanabe T, Seo S, Sakai S (2001) Wound-induced expression of a gene for 1-aminocyclopropane-1-carboxylate synthase and ethylene production are regulated by both reactive oxygen species and jasmonic acid in Cucurbita maxima. Plant Physiol Biochem 39:121–127

    Article  CAS  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Messrs. Minoru Yamamoto of Organic Farm Tsukuba and Rikio Hashimoto for providing their organic vegetables, and Dr. Tsutae Ito of NARO Institute of Fruit Tree Science for providing various apple products. We also thank Drs. Takayuki Mitsunaga and Toshiro Matsunaga of NARO Agricultural Research Center for their support with statistical analysis and valuable discussions, respectively. We gratefully acknowledge the assistance of experiments by Ms. Setsuko Tanaka and Ms. Yumiko Sasaki. This work was supported by Japan Society for the promotion of Science (JSPS) KAKENHI Grant Number 25660033.

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Correspondence to Fukuyo Tanaka.

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Responsible Editor: Eric J.W. Visser.

An erratum to this article can be found at http://dx.doi.org/10.1007/s11104-016-2866-5.

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Matsuoka, H., Ohwaki, Y., Terakado-Tonooka, J. et al. Changes in volatiles in carrots inoculated with ACC deaminase-producing bacteria isolated from organic crops. Plant Soil 407, 173–186 (2016). https://doi.org/10.1007/s11104-015-2769-x

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